Abstract
The aim of this study was to evaluate enzymatic (glutathione-S-transferase and catalase) and histological (branchial lesions) biomarkers in Ucides cordatus (Crustacea, Decapoda) from an industrial port region on the north coast of Brazil. The crabs were collected in two distinct locations of the Brazilian coast: A1 = region under influence of port activities; and A2 = low-impacted area. We performed histological examination in the gills and glutathione-S-transferase (GST) and catalase activity in the hepatopancreas. The most frequent and severe histological lesions were found in A1, especially rupture of pilaster cells and lamellar collapse. Catalase activity did not show a pattern capable of differentiating the two analyzed areas. On the other hand, GST activity presented a more pronounced response in the crabs of the port area (p < 0.05), coinciding with the most frequent branchial lesions in these same organisms. These results suggest that the species is susceptible to environmental stress, once alterations at different organizational levels were verified.
Similar content being viewed by others
References
Abdel-Khalek AA, Elhaddad E, Mamdouh S et al (2018) The chronic exposure to discharges of sabal drain induces oxidative stress and histopathological alterations in Oreochromis niloticus. Bull Environ Contam Toxicol 0:1–7. https://doi.org/10.1007/s00128-018-2366-9
Aly W, Williams ID, Hudson MD (2014) Limitations of metallothioneins in common cockles (Cerastoderma edule) and sponges (Haliclona oculata) as biomarkers of metal contamination in a semi-enclosed coastal area. Sci Total Environ 473–474:391–397. https://doi.org/10.1016/j.scitotenv.2013.11.136
Amaral R, Alfredin P (2010) Modelação Hidrossedimentológica no Canal de Acesso do Complexo Portuário do Maranhão. Rev Bras Recur Hídricos 15:5–14. https://doi.org/10.21168/rbrh.v15n2.p5-14
Ameur WB, El Megdiche Y, Lapuente J et al (2015) Oxidative stress, genotoxicity and histopathology biomarker responses in Mugil cephalus and Dicentrarchus labrax gill exposed to persistent pollutants. A field study in the Bizerte Lagoon: Tunisia. Chemosphere 135:67–74. https://doi.org/10.1016/j.chemosphere.2015.02.050
Andrade TSOM (2016) Biomarcadores em caranguejo uçá (Ucides cordatus) para monitoramento ambiental em áreas portuárias. Universidade Estadual do Maranhão
Arockia Vasanthi L, Muruganandam A, Revathi P et al (2014) The application of histo-cytopathological biomarkers in the mud crab Scylla serrata (Forskal) to assess heavy metal toxicity in Pulicat Lake, Chennai. Mar Pollut Bull 81:85–93. https://doi.org/10.1016/j.marpolbul.2014.02.016
Burggren WW, McMahon BR (1988) Biology of the Land Crabs. Cambridge University Press, Cambridge
Burton JE, Dorociak IR, Schwedler TE, Rice CD (2002) Circulating lysozyme and hepatic CYP1A activities during a chronic dietary exposure to tributyltin (TBT) and 3,3′,4,4′,5-pentachlorobiphenyl (PCB-126) mixtures in channel catfish, Ictalurus punctatus. J Toxicol Environ Heal - Part A 65:589–602. https://doi.org/10.1080/152873902317349745
Camargo MMP, Martinez CBR (2006) Biochemical and physiological biomarkers in Prochilodus lineatus submitted to in situ tests in an urban stream in southern Brazil. Environ Toxicol Pharmacol 21:61–69. https://doi.org/10.1016/j.etap.2005.07.016
Carvalho-Neta RNF, Abreu-Silva AL (2013) Glutathione S-transferase as biomarker in Sciades herzbergii (Siluriformes: Ariidae) for environmental monitoring: the case study of São Marcos Bay, Maranhão, Brazil. Lat Am J Aquat 41:217–225. https://doi.org/10.3856/vol41-issue2-fulltext-2
Carvalho-Neta RNF, Torres AR, Abreu-Silva AL (2012) Biomarkers in catfish Sciades herzbergii (Teleostei: Ariidae) from polluted and non-polluted areas (São Marcos’ Bay, Northeastern Brazil). Appl Biochem Biotechnol 166:1314–1327. https://doi.org/10.1007/s12010-011-9519-1
Carvalho-Neta RNF, Pinheiro-Sousa DB, Almeida Z da S de et al (2014) A histopathological and biometric comparison between catfish (Pisces, Ariidae) from a harbor and a protected area, Brazil. Aquat Biosyst 10:1–8. https://doi.org/10.1186/s12999-014-0012-5
Carvalho-Neta RNF, Torres AR, Sousa DBP et al (2016) In situ assessment of two catfish species (pisces, Ariidae) to evaluate pollution in a harbor. p 100007. https://doi.org/10.1063/1.4968699
Castro ACL (2001) Diversidade da assembléia de peixes em igarapés do estuário do rio Paciência (Ma–Brasil). Atlântica 23:39–46. https://doi.org/10.1590/S1676-06032008000200012
Contreras-Vergara CA, Harris-Valle C, Sotelo-Mundo RR, Yepiz-Plascencia G (2004) A mu-class glutathione-S-transferase from the marine shrimp Litopenaeus vannamei: molecular cloning and active-site structural modeling. J Biochem Mol Toxicol 18:245–252. https://doi.org/10.1002/jbt.20033
Cutrim AST, Sousa LKS, Oliveira VM, Almeida ZS (2016) Estrutura da comunidade de poliquetas em manguezais do Golfão Maranhense. In: Almeida ZS, Oliveira VM (eds) Avaliação Ambiental no Complexo Portuário do Itaqui. EDUEMA, São Luís, pp 145–165
Depledge MH (1994) The rational basis for the use of biomarkers as ecotoxicological tools. In: Fossi MC, Leonzio C (eds) Non-destructive biomarkers in vertebrates. Lewis, Boca Raton, pp 261–285
Freire MM, Santos VG, Ginuino ISF, Arias ARL (2008) Biomarcadores na avaliação da saúde ambiental dos ecossistemas aquáticos. Oecol Bras 12:347–354. https://doi.org/10.4257/oeco.2008.1203.01
Ighodaro OM, Akinloye OA (2018) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alex J Me 54:287–293. https://doi.org/10.1016/j.ajme.2017.09.001
Instituto Nacional de Meteorologia (INMET) (2017) Normal Climatológica do Brasil 1961–1990. http://www.inmet.gov.br/portal/index.php?r=clima/normaisClimatologicas. Accessed 28 Nov 2017
Jena KB, Verlecar XN, Chainy GBN (2009) Application of oxidative stress indices in natural populations of Perna viridis as biomarker of environmental pollution. Mar Pollut Bull 58:107–113. https://doi.org/10.1016/j.marpolbul.2008.08.018
Keen JH, Habig WH, Jakoby WB (1976) Mechanism for several activities of the glutathione-S-transferase. J Biol Chem 251:6183–6188
Krifka S, Spagnuolo G, Schmalz G, Schweikl H (2013) A review of adaptive mechanisms in cell responses towards oxidative stress caused by dental resin monomers. Biomaterials 34:4555–4563. https://doi.org/10.1016/j.biomaterials.2013.03.019
Lacroix C, Richard G, Seguineau C et al (2015) Active and passive biomonitoring suggest metabolic adaptation in blue mussels (Mytilus spp.) chronically exposed to a moderate contamination in Brest harbor (France). Aquat Toxicol 162:126–137. https://doi.org/10.1016/j.aquatox.2015.03.008
Lam PK, Gray JS (2003) The use of biomarkers in environmental monitoring programmes. Mar Pollut Bull 46:182–186. https://doi.org/10.1016/S0025-326X(02)00449-6
Macêdo SJ, Montes MJF, Lins IC (2002) Características abióticas da área. In: Barros HM, Eskinazi-Leça H, Macêdo SJ, Lima T (eds) Gerenciamento participativo de estuários e manguezais. Ed. Universitária da UFPE, Recife, p 252
Maharajan A, Narayanasamy Y, Ganapiriya V, Shanmugavel K (2015) Histological alterations of a combination of Chlorpyrifos and Cypermethrin (Nurocombi) insecticide in the fresh water crab, Paratelphusa jacquemontii (Rathbun). J Basic Appl Zool 72:104–112. https://doi.org/10.1016/j.jobaz.2015.08.002
Martín-Díaz ML, Blasco J, Sales D, DelValls TA (2008) Field validation of a battery of biomarkers to assess sediment quality in Spanish ports. Environ Pollut 151:631–640. https://doi.org/10.1016/j.envpol.2007.03.019
Moschino V, Del Negro P, Vittor C, Da Ros L (2016) Biomonitoring of a polluted coastal area (Bay of Muggia, Northern Adriatic Sea): a five-year study using transplanted mussels. Ecotoxicol Environ Saf 128:1–10. https://doi.org/10.1016/j.ecoenv.2016.02.006
Moureaux C, Simon J, Mannaerts G et al (2011) Effects of field contamination by metals (Cd, Cu, Pb, Zn) on biometry and mechanics of echinoderm ossicles. Aquat Toxicol 105:698–707. https://doi.org/10.1016/j.aquatox.2011.09.007
Negro CL (2015) Histopathological effects of endosulfan to hepatopancreas, gills and ovary of the freshwater crab Zilchiopsis collastinensis (Decapoda: Trichodactylidae). Ecotoxicol Environ Saf 113:87–94. https://doi.org/10.1016/j.ecoenv.2014.11.025
Negro CL, Collins P (2017) Histopathological effects of chlorpyrifos on the gills, hepatopancreas and gonads of the freshwater crab Zilchiopsis collastinensis. Persistent effects after exposure. Ecotoxicol Environ Saf 140:116–122. https://doi.org/10.1016/j.ecoenv.2017.02.030
Oliveira-Ribeiro CA, Narciso MF (2014) Histopathological markers in fish health assessment. In: Almeida EA, Oliveira-Ribeiro CA (eds) Pollution and fish health in tropical ecosystems. CRC Press, Boca Raton, pp 206–242
Olson KR (1991) Vasculature of the fish gill: anatomical correlates of physiological functions. J Electron Microsc Tech 19:389–405. https://doi.org/10.1002/jemt.1060190402
Ozkan D, Dagdeviren M, Katalay S et al (2017) Multi-biomarker responses after exposure to pollution in the Mediterranean Mussels (Mytilus galloprovincialis L.) in the Aegean Coast of Turkey. Bull Environ Contam Toxicol 98:46–52. https://doi.org/10.1007/s00128-016-1988-z
Paital B, Chainy GBN (2013) Seasonal variability of antioxidant biomarkers in mud crabs (Scylla serrata). Ecotoxicol Environ Saf 87: 33–41. https://doi.org/10.1016/j.ecoenv.2012.10.006
Pinheiro MAA, Fiscarelli AG (2001) Manual de Apoio á Fiscalização - Caranguejo-Uçá. Itajai
Pinheiro-Sousa DB, Almeida ZS de, Carvalho-Neta RNF (2013) Integrated analysis of two biomarkers in Sciades herzbergii (Ariidae, Siluriformes), to assess the environmental impact at São Marcos’ Bay, Maranhao, Brazil. Lat Am J Aquat Res 41:305–312. https://doi.org/10.3856/vol41-issue2-fulltext-9
Rebelo M, de F, Rodriguez, Santos EM, Ansaldo EA M (2000) Histopathological changes in gills of the estuarine crab Chasmagnathus granulata (Crustacea-Decapoda) following acute exposure to ammonia. Comp Biochem Physiol Part C 125:157–164. https://doi.org/10.1016/S0742-8413(99)00093-6
Rocha da CHS (2017) Bioacumulação de metais e presença de metalotioneína no caranguejo-uçá, Ucides cordatus (Linnaeus, 1763). Universidade Federal do Maranhão
Romano N, Zeng C (2012) Osmoregulation in decapod crustaceans: implications to aquaculture productivity, methods for potential improvement and interactions with elevated ammonia exposure. Aquaculture 334(1):12–23. https://doi.org/10.1016/j.aquaculture.2011.12.035
Santana MS, Yamamoto FY, Sandrini-Neto L et al (2018) Diffuse sources of contamination in freshwater fish: detecting effects through active biomonitoring and multi-biomarker approaches. Ecotoxicol Environ Saf 149:173–181. https://doi.org/10.1016/j.ecoenv.2017.11.036
Santos RM, Weber L, Souza VL et al (2016) Effects of water-soluble fraction of petroleum on growth and prey consumption of juvenile Hoplias aff. malabaricus (Osteichthyes: Erythrinidae). Braz J Biol 76:10–17. https://doi.org/10.1590/1519-6984.06714
Silva AC, França NS, Moreira EG (2016) Teor metálico em um manguezal sob influência portuária, São Luís, MA. In: Almeida ZS, Oliveira VM (eds) Avaliação Ambiental no Complexo Portuário do Itaqui. EDUEMA, São Luís, pp 167–195
Sousa DBP, Almeida ZS, Carvalho-Neta RNF (2013) Biomarcadores histológicos em duas espécies de bagres estuarinos da Costa Maranhense, Brasil. Arq Bras Med Vet Zootec 65:369–376. https://doi.org/10.1590/S0102-09352013000200011
Sousa LKS, Cutrim AST, Oliveira VM, Almeida ZS (2016) Poliquetas como indicadores da qualidade ambiental em manguezais do Golfão Maranhense, Brasil. In: Almeida ZS, Oliveira VM (eds) Avaliação Ambiental no Complexo Portuário do Itaqui. EDUEMA, São Luís, pp 11–33
Tagliari KC, Cecchini R, Rocha JAV, Vargas VMF (2004) Mutagenicity of sediment and biomarkers of oxidative stress in fish from aquatic environments under the influence of tanneries. Mutat Res 561:101–117. https://doi.org/10.1016/j.mrgentox.2004.04.001
United States Environmental Protection Agency: U.S.EPA (2007) SW-846 Test Method 3051: microwave assisted acid digestion of sediments, sludges, soils, and oils. https://www.epa.gov/hw-sw846/sw-846-test-method-3051a-microwave-assisted-acid-digestion-sediments-sludges-soils-and-oils. Accessed 21 Dec 2017
Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf 64:178–189. https://doi.org/10.1016/j.ecoenv.2005.03.013
Ventura EC, Gaelzer LR, Zanette J et al (2002) Biochemical indicators of contaminant exposure in spotted pigfish (Orthopristis ruber) caught at three bays of Rio de Janeiro coast. Mar Environ Res 54:775–779. https://doi.org/10.1016/S0141-1136(02)00137-X
Vieira RHSF, De Lima EA, Sousa DBR et al (2004) Vibrio spp. and Salmonella spp., presence and susceptibility in crabs Ucides cordatus. Rev Inst Med Trop Sao Paulo 46:179–182. https://doi.org/10.1590/S0036-46652004000400001
Welsh JE, King PA, MacCarthy E (2013) Pathological and physiological effects of nicking on brown crab (Cancer pagurus) in the Irish crustacean fishery. J Invertebr Pathol 112:49–56. https://doi.org/10.1016/j.jip.2012.08.006
Winkaler EU, Silva ADG, Galindo HC, Martinez CBDR (2008) Biomarcadores histológicos e fisiológicos para o monitoramento da saúde de peixes de ribeirões de Londrina, Estado do Paraná. Acta Sci Biol Sci 23:507–514. https://doi.org/10.4025/actascibiolsci.v23i0.2708
Zanette J, Monserrat JM, Bianchini A (2006) Biochemical biomarkers in gills of mangrove oyster Crassostrea rhizophorae from three Brazilian estuaries. Comp Biochem Physiol 143:187–195. https://doi.org/10.1016/j.cbpc.2006.02.001
Acknowledgements
The authors would like to acknowledge the research team of the Laboratory of Biomarkers in Aquatic Organisms (LABOAq) of the State University of Maranhão, for the support in the biological analyzes and the Foundation of Support to the Research and the Scientific and Technological Development of Maranhão (FAPEMA), for the financial support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
de Oliveira, S.R.S., Batista, W.S., Sousa, J.B.M. et al. Enzymatic and Histological Biomarkers in Ucides cordatus (Crustacea, Decapoda) in an Industrial Port on the North Coast of Brazil. Bull Environ Contam Toxicol 102, 802–810 (2019). https://doi.org/10.1007/s00128-019-02594-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00128-019-02594-1